*Corresponding author: KB McCune (kelseybmccune@gmail.com)
Cite as: Berens JM, Logan CJ, Folsom M, Sevchik A, Bergeron L, McCune KB. Submitted to PCI Ecology Nov 2020. Validating morphological condition indices and their relationship with reproductive success in great-tailed grackles.
This preregistration has been pre-study peer reviewed and received an In Principle Acceptance by:
Marcos Mendez (2019 In Principle Acceptance) Are condition indices positively related to each other and to fitness?: a test with grackles. Peer Community in Ecology, 100035. 10.24072/pci.ecology.100035
Morphological variation among individuals has the potential to influence multiple life history characteristics such as dispersal, migration, reproductive success, and survival (Wilder et al. 2016). Individuals that are in better “condition” can disperse or migrate further or more successfully, have greater reproductive success, and survive longer (Heidinger et al. 2010; Liao et al. 2011; Wilder et al. 2016), particularly in years where environmental conditions are harsh (Milenkaya et al. 2015). Body condition is defined in various ways, but is most often measured using an individual’s energetic or immune state (Milenkaya et al. 2015). These traits are difficult to measure directly, therefore a variety of morphological proxies to quantify condition are used instead, including fat score (Kaiser 1993), weight, ratio of weight to tarsus length (Labocha et al. 2014), a scaled mass index (Peig and Green 2009), as well as hematological indices for immune system function (Fleskes et al. 2017; Kraft et al. 2019). However, there is mixed support regarding whether these condition indices relate to life history characteristics (Labocha et al. 2014; Wilder et al. 2016), and whether the relationship is linear (McNamara et al. 2005; Milenkaya et al. 2015). Additionally, although some investigations use multiple morphological proxies for condition (e.g. Warnock and Bishop 1998), rarely have there been direct comparisons among proxies to validate that they measure the same trait. In this investigation, we define condition as an energetic state and we attempt to measure it by comparing two indices (fat score and the scaled mass index) to validate whether they measure the same trait and whether they correlate with measures of reproductive success in our study system, the great-tailed grackle (Quiscalus mexicanus). We found that the morphological proxies did not correlate with each other, indicating that they do not measure the same trait. Further, neither proxy correlated with reproductive success in males, measured as whether a male held a territory containing nests or not. We found that females with a high scaled mass index had a significantly lower probability that their nest would survive on any given day. However, there was no relationship between female fat score and nest survival. These results indicate that measures of condition should be validated before relying on their use as a condition proxy in grackles and birds in general. Future research should further investigate our unexpected result that higher scaled mass index correlated with lower nest survival to better understand the importance of energetic condition for reproductive success - a necessary component for selection to act.
Morphological variation among individuals has the potential to influence multiple life history characteristics such as dispersal, migration, reproductive fitness, and survival (Wilder et al. 2016). One morphological trait that might be particularly likely to influence these life history characteristics is energetic condition. Individuals that are in better “condition” can disperse or migrate further or more successfully, have greater reproductive success, and survive longer (Heidinger et al. 2010; Liao et al. 2011; Wilder et al. 2016), particularly in years where environmental conditions are harsh (Milenkaya et al. 2015). For example, a study conducted on vipers showed that while the level of fat reserves in males was not related to their sexual activity, females with low fat reserves engaged in sexual interactions less frequently than those with higher fat reserves (Aubret et al. 2002). In contrast, mantids showed conflicting results regarding the relationship between fat reserves and reproductive success (Barry and Wilder 2013). Female mantids were fed either a high protein, low lipid diet, or a high lipid, low protein diet. The females that received the high lipid diet had higher lipid content in most parts of their body compared to that of their high protein diet counterparts. However, they were not able to produce even half as many eggs as the females fed the high protein, low lipid diet. This led to lower male attraction, measured by the number of copulation events, thus negatively impacting further reproductive success.
A variety of morphological proxies have been used to quantify energetic condition (i.e., fat score, weight, ratio of weight to tarsus length, ratio of weight to wing chord length; Labocha et al. 2014). However, there is mixed support regarding whether and how these proxies relate to life history characteristics (Labocha et al. 2014; Wilder et al. 2016). A review conducted by Barnett (2015) shows that, while mass or body size measures of condition are often assumed to have a positive linear relationship with fitness, this is not always the case, and the relationship should first be empirically validated before being used as a proxy (Barnett et al. 2015). In some instances, the condition proxy might relate to life history characteristics, but in an unexpected way. For example, theoretical simulations of small birds show that survival does not increase linearly with energy (i.e., fat) reserves (McNamara et al. 2005). If the reserves are too low, the individual is at risk of starvation. However, once the reserves get too high, the individual is at an increased risk of predation (McNamara et al. 2005). Thus, fat reserves can relate to a life history variable (survival), but in a U-shaped relationship rather than a linear one.
Although some studies use multiple morphological proxies for condition (e.g., Warnock and Bishop 1998), rarely are these variables directly compared. Multiple proxies should correlate with each other if they measure the same trait (energetic condition). Furthermore, there is still confusion about what trait some proxies actually measure. For example, a study conducted on two species of crickets showed that three estimates of body condition based on fat content or on the relationship between body mass and body length (scaled mass index or ordinary least squares regression) did not correlate with each other (Kelly et al. 2014), thus indicating that they do not measure the same trait. This is an example of the jingle fallacy (Block 1995; Carter et al. 2013), where a single trait label (“condition”) actually encompasses more than one distinct trait. In this case, two investigations using different proxies can be conducted on the same research question, using the same species, but may end up with different results. This is problematic because inconsistency in results among researchers can result in potentially misleading interpretations of the impact of variation in morphology in relation to life history and population variables (Stevenson and Woods Jr 2006).
Here we compare two indices (fat score and the scaled mass index) of an individual’s energetic state to validate whether they correlate with each other, which would indicate that they both measure body condition. Fat score, as described by Kaiser (1993), is a numerical estimate of the amount of fat visible under the skin (Fig. 1). The score ranges from 0 to 8 depending on the size and appearance of the fat located in the individual’s abdomen and interclavicular depression, with 0 indicating no visible fat and 8 indicating extensive fat covering the ventral surface such that no muscle tissue is visible. For example, a score of 1 corresponds to sparse traces of fat visible in the interclavicular depression and abdomen. This measure is frequently used in birds (Merilä and Svensson 1997; Erciyas et al. 2010; Cornelius Ruhs et al. 2019), and is a straightforward, non-invasive method for estimating condition. However, previous research found that it does not always positively relate with life history variables. For example, Haas (1998) found no difference between fat scores in individuals that had successful or failed nests in American robins and brown thrashers, indicating that fat score may not explain much of the variation in nest success in some species. Further research is needed to understand the relationship between fat score measures and life history characteristics.
In contrast, the scaled mass index (SMI) is more difficult to calculate than the fat score, but it has become the predominant ratio method for quantifying energetic condition within and among populations (Maceda-Veiga et al. 2014; Delciellos et al. 2018; English et al. 2018). The SMI is an individual’s mass scaled by skeletal body size (Peig and Green 2009). Unlike the common alternative which uses a simple ratio of tarsus (lower leg) length to body mass, the SMI accounts for the tendency towards allometric scaling where the relationship between body mass and structural size increases by a power law (Huxley 1932). When individuals with different structural body sizes can be standardized to the population average structural body size, then energetic condition (the amount of mass not explained by structural body size) can be more directly compared within and across populations. That is, the SMI calculates the energetic condition as the mass of an individual relative to the population by first computing the mass that the individual would have at the population average of a specific body measurement (e.g., tarsus length). Next, structural body size of the individual is standardized by scaling the individual’s structural body length by the population average of that body measurement, which accounts for population differences. The SMI is calculated as: \(Mass_i\left[ \frac{AvgLength_p}{Length_i} \right]^{slope_p}\) where \(Mass_i\) is each individual’s weight in grams, \(Length_i\) is the value of the chosen measure of structural body length for each bird, \(AvgLength_p\) is the average structural body length in the population, and \(slope_p\) is calculated from the standard major axis regression (which is used to compare variables that were both directly measured and thus have residual error) of a structural body size measure, like tarsus length, on mass (Peig and Green 2009), and is interpreted as the expected change in structural length for a one unit increase in mass. Therefore, individuals in better energetic condition (larger weight for their structural body size) will have a higher SMI compared to individuals in poor condition. Studies across taxa found that the SMI relates positively to reproductive success and survival. For example, mallards with a lower SMI had lower rates of survival compared to their higher SMI counterparts (Champagnon et al. 2012), while in crimson finches SMI was positively related to the number of young that survived to independence (Milenkaya et al. 2015).
Our research will determine whether these two indices of energetic condition measure the same trait, and whether this trait relates to an important life history characteristic: reproductive success. Measuring reproductive success in birds involves finding and monitoring nests (Mayfield 1961). However, nests are usually built in cryptic locations and parents behave secretly (Gill 1995), thus making it difficult to quantify the number of eggs and nestlings inside the nest over time. Additionally, it is difficult and time-consuming to track the survival of offspring once they leave the nest. Therefore, we will use the predominant method in this field for quantifying reproductive success: whether a nest fledged offspring (Mayfield 1961).
Our study system is a population of great-tailed grackles (Quiscalus mexicanus), hereafter “grackles”, in Tempe, Arizona. This system is ideal for this investigation because grackles are native to the tropical climates of Central America (Johnson and Peer 2001), but have rapidly expanded their geographic range into new areas (Wehtje 2003). Because grackles are a water-associated species, the desert habitat of Tempe presents physiological challenges that could lead to an increased likelihood of a tradeoff between survival and reproductive attempts (Henderson et al. 2017). Deserts are characterized by a scarcity of water and extreme temperature fluctuations, which require behavioral and physiological adaptations (Costa 2012). Wide variation in body condition and reproductive success is possible if grackle physiology requires more water than is present in the environment, and some individuals may cope with physiological stress, or find hidden sources of water, better than others (Henderson et al. 2017).